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Frankia Root Hair Deforming Factor Shares Actinorhizal signaling molecules : Frankia root hair deforming factor shares properties with NIN inducing factor Maimouna Cissoko, Valérie Hocher, Hassen Gherbi, Djamel Gully, Alyssa Carré-Mlouka, Seyni Sane, Sarah Pignoly, Antony Champion, Mariama Ngom, Petar Pujic, et al. To cite this version: Maimouna Cissoko, Valérie Hocher, Hassen Gherbi, Djamel Gully, Alyssa Carré-Mlouka, et al.. Acti- norhizal signaling molecules : Frankia root hair deforming factor shares properties with NIN inducing factor. Frontiers in Plant Science, Frontiers, 2018, 9, 12 p. 10.3389/fpls.2018.01494. hal-01956101 HAL Id: hal-01956101 https://hal.archives-ouvertes.fr/hal-01956101 Submitted on 14 Dec 2018 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Distributed under a Creative Commons Attribution| 4.0 International License fpls-09-01494 October 16, 2018 Time: 19:31 # 1 ORIGINAL RESEARCH published: 18 October 2018 doi: 10.3389/fpls.2018.01494 Actinorhizal Signaling Molecules: Frankia Root Hair Deforming Factor Shares Properties With NIN Inducing Factor Maimouna Cissoko1,2,3,4, Valérie Hocher4, Hassen Gherbi4, Djamel Gully4, Alyssa Carré-Mlouka4,5, Seyni Sane6, Sarah Pignoly1,2,4, Antony Champion1,2,7, Mariama Ngom1,2, Petar Pujic8, Pascale Fournier8, Maher Gtari9, Erik Swanson10, Céline Pesce10, Louis S. Tisa10, Mame Oureye Sy3 and Sergio Svistoonoff1,2,4* 1 Laboratoire Commun de Microbiologie, Institut de Recherche pour le Développement/Institut Sénégalais de Recherches Agricoles/Université Cheikh Anta Diop, Centre de Recherche de Bel Air, Dakar, Senegal, 2 Laboratoire Mixte International Adaptation des Plantes et Microorganismes Associés Aux Stress Environnementaux, Centre de Recherche de Bel Air, Dakar, Senegal, 3 Laboratoire Campus de Biotechnologies Végétales, Département de Biologie Végétale, Faculté des Sciences et Techniques, Université Cheikh Anta Diop, Dakar, Senegal, 4 Laboratoire des Symbioses Tropicales et Méditerranéennes, Institut de Recherche pour le Développement/INRA/CIRAD, Université Montpellier/SupAgro, Montpellier, France, 5 UMR 7245, Molécules de Communication et Adaptation des Microorganismes, Muséum National d’Histoire Naturelle, Centre National de la Recherche Scientifique, Sorbonne Universités, Paris, France, 6 Laboratoire de Botanique et de Biodiversité Végétale, Département de Biologie Végétale, Faculté des Sciences et Techniques, Université Cheikh Anta Diop, Dakar, Edited by: Senegal, 7 UMR Diversité Adaptation et Développement des Plantes (DIADE), Institut de Recherche pour le Développement, Ulrike Mathesius, Montpellier, France, 8 Ecologie Microbienne, UMR 5557 CNRS, Université Lyon 1, Villeurbanne, France, 9 Institut National Australian National University, des Sciences Appliquées et de Technologie, Université Carthage, Tunis, Tunisia, 10 Department of Molecular, Cellular, Australia and Biomedical Sciences, University of New Hampshire, Durham, NH, United States Reviewed by: Dugald Reid, Aarhus University, Denmark Actinorhizal plants are able to establish a symbiotic relationship with Frankia bacteria Ton Bisseling, leading to the formation of root nodules. The symbiotic interaction starts with the Wageningen University & Research, Netherlands exchange of symbiotic signals in the soil between the plant and the bacteria. This *Correspondence: molecular dialog involves signaling molecules that are responsible for the specific Sergio Svistoonoff recognition of the plant host and its endosymbiont. Here we studied two factors [email protected] potentially involved in signaling between Frankia casuarinae and its actinorhizal host Specialty section: Casuarina glauca: (1) the Root Hair Deforming Factor (CgRHDF) detected using a This article was submitted to test based on the characteristic deformation of C. glauca root hairs inoculated with Plant Evolution and Development, F. casuarinae and (2) a NIN activating factor (CgNINA) which is able to activate a section of the journal Frontiers in Plant Science the expression of CgNIN, a symbiotic gene expressed during preinfection stages Received: 31 May 2018 of root hair development. We showed that CgRHDF and CgNINA corresponded to Accepted: 25 September 2018 small thermoresistant molecules. Both factors were also hydrophilic and resistant to Published: 18 October 2018 a chitinase digestion indicating structural differences from rhizobial Nod factors (NFs) or Citation: Cissoko M, Hocher V, Gherbi H, mycorrhizal Myc-LCOs. We also investigated the presence of CgNINA and CgRHDF in Gully D, Carré-Mlouka A, Sane S, 16 Frankia strains representative of Frankia diversity. High levels of root hair deformation Pignoly S, Champion A, Ngom M, (RHD) and activation of ProCgNIN were detected for Casuarina-infective strains from Pujic P, Fournier P, Gtari M, Swanson E, Pesce C, Tisa LS, Sy MO clade Ic and closely related strains from clade Ia unable to nodulate C. glauca. Lower and Svistoonoff S (2018) Actinorhizal levels were present for distantly related strains belonging to clade III. No CgRHDF or Signaling Molecules: Frankia Root Hair Deforming Factor Shares CgNINA could be detected for Frankia coriariae (Clade II) or for uninfective strains from Properties With NIN Inducing Factor. clade IV. Front. Plant Sci. 9:1494. doi: 10.3389/fpls.2018.01494 Keywords: symbioses, nodulation factors, nodule inception, Casuarina, Alnus, Discaria Frontiers in Plant Science| www.frontiersin.org 1 October 2018| Volume 9| Article 1494 fpls-09-01494 October 16, 2018 Time: 19:31 # 2 Cissoko et al. Properties of Actinorhizal Signaling Molecules INTRODUCTION Much less is known about signaling molecules involved in the actinorhizal symbioses. Canonical nodABC genes are not Legumes and actinorhizal plants form a N2-fixing root nodule found in the sequenced genomes of 36 Frankia strains including symbiosis in association with rhizobia and Frankia bacteria, Frankia alni and Frankia casuarinae (Tisa et al., 2016) confirming respectively (Vessey et al., 2005). The establishment of these a previous report showing that F. alni DNA will not complement beneficial bacterial-plant relationships requires communication rhizobial nod mutants (Cérémonie et al., 1998). Only distant between the partners. Rhizobial symbioses have received homologs of nodB and nodC are found in F. alni genome. Unlike considerable attention because several legumes are important rhizobial nod genes, they are not organized into a cluster together crop species. However, actinorhizal symbioses, which play an with other symbiotic genes and their expression is not induced important ecological role (Dawson, 2008), have been less well under symbiotic conditions (Normand et al., 2007; Alloisio studied and the molecular dialog between Frankia and their et al., 2010). These findings are consistent with experiments host plants is still poorly understood. One reason is that showing that chitin oligomers similar to rhizobial NFs are not be most actinorhizal plants are woody shrubs or trees for which detected in F. alni culture supernatant (Cérémonie et al., 1999) genetic approaches are very difficult (Wall, 2000; Perrine-Walker suggesting structural differences between the Frankia symbiotic et al., 2011). In addition, the genetics of the bacterial partner, signals and rhizobial NFs. Recently, canonical nodABC genes Frankia, is not fully developed and up to now Frankia cells have been found in the genome of two uncultured Frankia remain recalcitrant to stable genetic transformation (Kucho strains: Candidatus Frankia datiscae Dg1 and Candidatus Frankia et al., 2009, 2017). Recent progress including the sequencing californicae Dg2 (Persson et al., 2015; Nguyen et al., 2016), and of several Frankia genomes (Normand et al., 2007; Tisa in one isolated strain, Frankia sp. NRRL B-16219 (Ktari et al., et al., 2016), transcriptomic studies (Alloisio et al., 2010; 2017). F. datiscae Dg1 nodABC genes are arranged in two operons Benson et al., 2011), proteomic studies (Mastronunzio and which are expressed in Datisca glomerata nodules, but their Benson, 2010; Ktari et al., 2017) together with functional involvement in symbiotic signaling is still not known (Persson studies on several actinorhizal species (Svistoonoff et al., et al., 2015). 2014) have opened new avenues for identifying components Frankia is able to infect their host root either through involved in the initial symbiotic dialog between the two intracellular (root hair) or intercellular modes. In the first case, partners. one of the earliest visible plant response to Frankia is an extensive The interaction of rhizobia with model legumes begins deformation of root hairs. This response occurs in actinorhizal with the production and recognition of signal molecules by plants belonging to the order Fagales (Betulaceae, Casuarinaceae) their respective eukaryotic and prokaryotic symbiotic partners that display a range of relatively advanced features reminiscent of (Oldroyd, 2013). Early events leading to nodule formation model legumes: a complex root hair infection process involving involve bacterial penetration into their hosts
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